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Effects of N:P:Si Ratios and Zooplankton Grazing on Phytoplankton Communities in the Northern Adriatic Sea

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Effects of N:P:Si Ratios and Zooplankton Grazing on Phytoplankton Communities in the Northern Adriatic Sea AQUATIC MICROBIAL ECOLOGY Vol. 18: 37-54, 1999 Published July 16 Aquat Microb Ecol 1 Effects of N:P:Si ratios and zooplankton grazing on phytoplankton communities in the northern Adriatic Sea. I. Nutrients, phytoplankton biomass, and polysaccharide production Edna Granelil.*, Per ~arlsson',Jefferson T. urne er^, Patricia A. ester^, Christian Bechemin4, Rodger ~awson',Enzo ~unari' 'University of Kalmar, Department of Marine Sciences. POB 905, S-391 29 Kalmar. Sweden 'Biology Department. University of Massachusetts Dartmouth. North Dartmouth, Massachusetts 02747. USA 3National Marine Fisheries Service, NOAA, Southeast Fisheries Science Center. Beaufort Laboratory, Beaufort. North Carolina 28516, USA 4CREMA-L'Houmeau(CNRS-IFREMER), BP5, F-17137 L'Houmeau, France 'Chesapeake Biological Laboratory, University of Maryland, Solomons, Maryland 20688. USA '~aboratoriodi Igiene Ambientale, Istituto di Sanita, Viale R. Elena 299. 1-00161 Rome, Italy ABSTRACT: The northern Adriatic Sea has been historically subjected to phosphorus and nitrogen loading. Recent signs of increasing eutrophication include oxygen def~ciencyin the bottom waters and large-scale formation of gelatinous macroaggregates. The reason for the formation of these macroag- gregates is unclear, but excess production of phytoplankton polysacchandes is suspected. In order to study the effect of different nutrient (nitrogen~phosphorus:silicon)ratios on phytoplankton production, biomass, polysacchandes, and species succession, 4 land-based enclosure experiments were per- formed with northern Adriatic seawater. During 2 of these experiments the importance of zooplankton grazlng as a phytoplankton loss factor was also investigated. Primary productivity in the northern Adri- atic Sea is thought to be phosphorus limited, and our experiments confirmed that even low daily phos- phorus additions Increased phytoplankton biomass. However, this only occurred when nitrogen addi- tions were high. Alternatively, when nitrogen was added in low concentrations, ulth simultaneous high phosphorus add~t~ons,phytoplankton biomass declined Nitrogen deficiency induced the highest pro- duction of polysacchandes per unit of cell carbon, while nutrient-sufficient and phosphorus-deficient treatments caused a higher production of polysaccharides in total. In order to decrease the frequency of algal blooms and high polysaccharide production in the northern Adnatic, it appears necessary to reduce the amounts of incoming nutrients. Since phosphorus has a high turnover rate in low P:high N waters of the northern Adnatic, and slnce our experiments show that a shortage of nitrogen can pro- duce reduced levels of phytoplankton biomass and total polysaccharides, a reduction of the nitrogen discharge would probably be the best countermeasure for eutrophicat~onIn the northern Adnatic Sea. KEY WORDS: Adriat~cSea. Nitrogen. Sdicon . Lunitation . Phytoplankton . Phosphorus. Polysaccharide Chemical composition INTRODUCTION Adriatic Sea has been undergoing eutrophication for decades due to large loadings of phosphorus (P) and Eutrophication due to anthropogenic nutrient load- nitrogen (N) originating from agriculture, industries ing in coastal marine waters is a growing problem and sewage (Justic 1987). Although anoxic events in throughout the world (Likens 1972, Caraco et al. 1990, the bottom waters of the northern Adriatic Sea have Nixon 1990, Vollenweider et al. 1992). The northern occurred sporadically for several centuries (Piccinetti & Manfrin 1969),the frequency of occurrence and size of 'E-mail: [email protected] se the areas exhibiting oxygen deficiency have dramati- O Inter-Research 1999 3 8 Aquat Microb Ecol 18: 37-54, 1999 Trieste For most marine coastal waters and inland seas N is thought to be the most limiting nutrient for phyto- plankton production (Ryther & Dunstan 1971, Howarth 1988, Graneli et al. 1990, Oviatt et al. 1995).However, a few cases have been reported where P limits produc- tion (Berland et al. 1980, Smith 1984), and P has been suggested to be limiting in marine coastal waters only when large nutrient loads with high N:P ratios reach PO river '~ \ '% coastal waters (Howarth 1988). Phosphorus has been suggested to be the most limit- ing nutrient for phytoplankton primary production in the northern Adriatic Sea. Indeed, 80% of the inor- ganic N:P ratios found in the surface waters suggest that P is limiting phytoplankton growth (Chiaudani et -Sampling al. 1980b),and bioassay experiments have confirmed a '9stat ion marked stimulation of phytoplankton growth when P was added (Pojed & Kveder 1977). The main objectives of our experiments were to Fig. 1. Location of the sampling station for the water used in investigate: (1) the effects of different N, P and silicon the enclosure experiments (Si) ratios and concentrations on phytoplankton growth, biomass, production, polysaccharide produc- cally increased during the last 2 decades (Justic 1987, tion, biochemical composition and changes in the 1991). intracellular content of carbon (C), N and P; (2) the Another possible sign of increasing eutrophication in effects of these nutrient manipulations on the abun- these waters is formation of gelatinous macroaggre- dance and composition of natural phytoplankton com- gates of huge proportions, known locally as 'mare munities; and (3) the impact of zooplankton grazing on sporco' or 'dirty water' (Stachowitsch et al. 1990, Mar- these phytoplankton communities. chetti 1992). These gelatinous masses are thought to Experiments were performed in May 1993, June be related to phytoplankton blooms, and have caused 1993, May 1994 and August 1994 in land-based enclo- beach fouling throughout the northern Adriatic Sea, sures in Fano, Italy. Nutrient, phytoplankton biomass, with substantial economical losses for an otherwise primary production and polysaccharide production flourishing tourism industry. These phenomena have results for the June 1993, May 1994 and August 1994 not been associated with severe oxygen deficiency, experiments will be presented in this paper. Effects of however, probably due to the low content of organic different nutrient ratios and concentrations on phyto- matter in the gelatinous mass (Marchetti 1992). How- plankton species composition in the June 1993 and ever, oxygen deficiency has been observed in the bot- May 1994 experiments will be presented in the second tom waters after large accumulations of gelatinous paper in this series (Carlsson & Graneli 1999, in this macroaggregates during the summers of 1988 and issue). Fluctuations of zooplankton in enclosures and 1989 (Degobbis 1989). Other harmful blooms occurring results of zooplankton grazing experiments from the in this area include those of toxic phytoplankton spe- May 1993 and June 1993 experiments will be pre- cies (Boni et al. 1993, Fonda Umani et al. 1993). sented in the third paper in this series (Turner et al. The main source of nutrients for the northern Adri- 1999, in this issue). atic Sea is the PO River (Degobbis & Gilmartin 1990, Vollenweider et al. 1992), with a mean discharge of about 1500 m3 S-' (Cati 1981) of water containing high MATERIALS AND METHODS concentrations of N and P. The total amount of P reach- ing the northern Adriatic is approximately 30000 tons Experiments were performed in land-based enclo- yr-l, of which the PO River contributes about 60% (Chi- sures using northern Adriatic seawater. The construc- audani & Vighi 1982). Approximately 152000 tons yr-' tion of this land-based enclosure system has been pre- of N reaches coastal waters, of which 75% is dis- viously described in Olsson et al. (1992). The water charged by the PO River (Chiaudani et al. 1980a). The containing the natural phytoplankton communities large transport of nutrients to the relatively shallow was pumped from 1 to 2 m depth from a station 15 km sea, markedly increases the primary production in off the east coast of Italy, offshore from Fano (Fig. l), these waters (Gilmartin & Revelante 1980, Malej et al. and filled into 500 1 dark-blue plastic containers. 1995). While filling the tanks on board the ship, the water Graneli et al.: Effects of nutrients and zooplankton grazing on phytoplankton. I 3 9 was filtered through 100 pm mesh in order to remove from the different 500 1 plastic transport containers extraneous mesozooplankton. We realized that this and any initial patchiness in the sampled water was sieving could also remove some chain-forming integrated. diatoms, if present, but since initial inspections After filling the cylinders with 100 1 of seawater, revealed that the phytoplankton was dominated by samples were taken from all the cylinders for immedi- small microflagellates, we considered that removal of ate analyses of nutrients (NOs, NH,, PO, and Si(OH),), extraneous grazers from the containers was more chlorophyll a (chl a), primary production, and particu- important than the error caused by possibly removing late C, N and P. The phytoplankton communities were some chain-forming diatoms. The containers were exposed to different N:P:Si regimes (Table 1).Based on lifted from the ship and placed on a truck for immedi- the concentrations found for the different nutrients in ate transport to the experimental site (this procedure the collected water, additions of PO,, NO, and Si(OH)4 lasted for about 1 h and there was no significant tem- were made to the different cylinders in order to obtain perature change in the water). The enclosures con- different nutrient ratios in the May 1994, June 1993, sisted of 100 1 white
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